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Article

Metagenomic Analysis of Garden Soil-Derived Microbial Consortia and Unveiling Their Metabolic Potential in Mitigating Toxic Hexavalent Chromium

by
Nidhi Singh
1,
Veer Singh
2,
Sachchida Nand Rai
3,
Emanuel Vamanu
4,* and
Mohan P. Singh
3,*
1
Centre of Bioinformatics, University of Allahabad, Prayagraj 211002, India
2
School of Biochemical Engineering, Indian Institute of Technology, Banaras Hindu University, Varanasi 221005, India
3
Centre of Biotechnology, University of Allahabad, Prayagraj 211002, India
4
Faculty of Biotechnology, University of Agricultural Sciences and Veterinary Medicine of Bucharest, 011464 Bucharest, Romania
*
Authors to whom correspondence should be addressed.
Life 2022, 12(12), 2094; https://doi.org/10.3390/life12122094
Submission received: 3 November 2022 / Revised: 7 December 2022 / Accepted: 11 December 2022 / Published: 13 December 2022
(This article belongs to the Special Issue Novel Insights into Phytoremediation of Pollutants)
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Abstract

:
Soil microbial communities connect to the functional environment and play an important role in the biogeochemical cycle and waste degradation. The current study evaluated the distribution of the core microbial population of garden soil in the Varanasi region of Uttar Pradesh, India and their metabolic potential for mitigating toxic hexavalent chromium from wastewater. Metagenomes contain 0.2 million reads and 56.5% GC content. The metagenomic analysis provided insight into the relative abundance of soil microbial communities and revealed the domination of around 200 bacterial species belonging to different phyla and four archaeal phyla. The top 10 abundant genera in garden soil were Gemmata, Planctomyces, Steroidobacter, Pirellula, Pedomicrobium, Rhodoplanes, Nitrospira Mycobacterium, Pseudonocardia, and Acinetobacter. In this study, Gemmata was dominating bacterial genera. Euryarchaeota, Parvarchaeota, and Crenarchaeota archaeal species were present with low abundance in soil samples. X-ray photoelectric spectroscopy (XPS) analysis indicates the presence of carbon, nitrogen–oxygen, calcium, phosphorous, and silica in the soil. Soil-derived bacterial consortia showed high hexavalent chromium [Cr (VI)] removal efficiency (99.37%). The bacterial consortia isolated from garden soil had an important role in the hexavalent chromium bioremediation, and thus, this study could be beneficial for the design of a heavy-metal treatment system.

1. Introduction

Microorganisms are the most abundant organism in the environment and are present everywhere on the earth, including solid waste, water, the human gut and soil ecosystems inhabited by an enormous plethora of microbial communities [1]. One soil sample predictably contains over 1030 microorganisms and thousands of archaea and eukaryotes [2]. In soil systems, the physiochemical properties of soil are influenced by bacterial communities [3]. Soil microbial communities are also affected by soil texture. The bacterial proportion is most dominant in the soil microbial communities [4,5]. The most common bacterial genera in grasslands are Acidobacteria, Actinobacteria, and Proteobacteria [6]. There are several studies on soil metagenomics that have been conducted, but only a few research studies have explained the role of soil microbial diversity in waste management and land use [7]. Land use has also been observed indirectly affecting the microbial community structure due to changes in soil characteristics such as pH, temperature, and elemental composition [8]. Some other factors, such as pesticides, fertilizer, and rainfall, also affect the soil microbial diversity [9].
Soil microbial diversity is very complex, and its culture is challenging for researchers. According to microbial evolutionary studies, about 1% of the bacterial species found in the environment can be cultured in the lab [10,11]. Various types of microbial diversity present in the soil are uncharacterized [12]. The metagenome approach is used to explain the core microbiota of many fields such as crops, soil, gut microbiome, wastewater, etc. [13]. Metagenomics is a culture-independent method used for the characterization of microbial diversity in soil samples [14]. It recognizes the diversity of uncultured soil microbial species by analyzing the direct isolation of genetic materials (DNA) from given habitats [15,16]. Rawat and Joshi [1] reported that Next-Generation-Sequencing technology has emerged as a valuable tool for analyzing biodiversity in metagenomic samples and metabolic pathways. Recently, the next-generation technique has been extensively used for microbial diversity analysis to address environmental concerns [17,18]. Next-generation sequencing (NGS) technologies that mark conserved regions of evolutionary indicators to find operational taxonomic units (OTUs) extend the analysis of complex microbial communities [19]. These approaches distinguish viruses, bacteria, fungi, parasites, and archaea from previously undiscovered and uncultivable organisms [20]. Soil microbial communities involve the highest level of prokaryote organisms in the environment [21].
Soil microbes, especially garden-soil microbes, have lignocellulosic degradation properties [22]. Soil microbes also play important role in suppressing plant diseases such as Clubroot disease, Root-Rot Disease, and Chinese Clubroot [23,24,25]. In addition, heavy metal-tolerant microbes isolated from soil have good heavy metal removal properties. It has been described that soil microbes encourage plant growth and enhance the phytoremediation of heavy metal ions [26]. Heavy metals such as arsenic (As), cadmium (Cd), chromium (Cr), lead (Pb), and mercury (Hg) cause several harmful effects such as kidney damage, heart failure, liver damage, and cancer [27,28,29]. Hexavalent chromium (Cr (VI)) is a carcinogenic heavy metal ion, and it has 100 times more toxicity than Cr (III) [30]. Cr (VI) comes in the effluent of several industrial activities such as chromate plating, leather tanneries, steel, and paint [31]. Several heavy-metal removal methods include reverse osmosis, chemical reduction, and precipitation use for the removal of Cr (VI) from wastewater [32]. These described heavy metal removal methods showed several limitations such as the production of secondary pollutants and the inability to remove heavy metals at very low concentrations of heavy-metal ions in the water [27,33]. Microbial removal of Cr (VI) is considered an eco-friendly, inexpensive and effective method. Several studies have been conducted on the microbial elimination of Cr (VI) from contaminated sites [34,35,36,37].
This study aimed to investigate the microbial diversity of garden soil. The elemental composition of the soil sample was also investigated. Additionally, the Cr (VI) removal efficiency of garden soil-derived microbial consortia was also explored in this study.

2. Materials and Methods

2.1. Sample Collection and Elemental Characterization

One garden soil sample was collected from the Banaras Hindu University campus, Varanasi, India (latitude 25°19′18.0624″ N, longitude 82°59′14.2404″ E) in November 2020. The temperature of the soil sample was 21 °C at the time of sample collection. The soil sample was stored at 4 °C in the laboratory until further analysis. The elemental composition, including phosphorus (P), calcium (Ca), nitrogen (N), silica (Si), and oxygen (O) was investigated through X-ray photoelectric spectroscopy (XPS) (Thermo Fisher Scientific make, Waltham, MA, USA). The sample for XPS analysis was prepared by mixing a 3:1 ratio of potassium dichromate (KBr) (HiMedia make, Mumbai, India) and soil sample [30].

2.2. DNA Extraction and Metagenomic Sequencing

The total DNA was extracted from a 1 g garden soil sample using commercially presented kits such as Qiagen, Zymo Research, and Thermo Fisher [38,39]. NanoDrop and gel electrophoresis were used to assess the quality of the extracted DNA [40]. The quality of DNA was estimated at 260/280 using NanoDrop, and the reading value aimed to stay in the range of 1.8 to 2. The DNA was amplified using polymerase chain reaction (PCR) at standard PCR conditions [40]. Primers 13F (5′AGAGTTTGATGMTGGCTCAG3′) and 13R (5′ TTACCGCGGCMGCSGGCAC3′) were used in PCR. The second nested PCR was used for the amplification of the entire variable region (V3-V4 hypervariable region) of 16S rDNA. The primers V13F (5′AGAGTTTGATGMTGGCTCAG3′) and V13R (5′ TTACCGCGGCMGCSGGCAC3′) were used for the amplification of the entire variable region. Eight further cycles of PCR were performed with Illumina barcoded adapters to prepare the sequencing libraries. AMPure beads were used to purify the libraries, and a Qubit dsDNA High-Sensitivity assay kit was used to quantify them. Next-generation sequencing was performed using an Illumina MiSeq with a 2x300 PE v3 sequencing kit.

2.3. Bioinformatics Analysis

The quality check of raw data was carried out using FastQC, then trimming low-quality reads using TRIMGALORE [41,42]. The trimmed reads were then processed further using the Uclust tool, which produced sequences that were combined and grouped into operational taxonomic units (OTUs), removed chimeras, and merged paired-end reads with an average 97% sequence similarity. An open-reference OTU was chosen and used to search the GreenGenes reference database [43]. QIIME2 workflows achieve OTU abundance calculation and estimation correction [44].

2.4. Isolation of Soil-Derived Microbial Consortia and Cr (VI) Removal Using Microbial Consortia

The mixed bacterial species were isolated from garden soil. First, 1 g of soil sample was mixed in 100 mL of Luria Bertani (LB) broth and incubated at 37 °C for 24 h. Next, 1 mL grown mixed bacterial culture was inoculated in Luria Bertani (LB) broth containing 100 mg/L Cr (VI). The effect of Cr (VI) on microbial growth was investigated for 24 h. The Cr (VI) removal efficiency of microbial consortia was also evaluated. The mixed bacterial culture was incubated for 6 days at pH 7, 37 °C, and 180 rpm. The samples were collected at 24 h intervals for 6 days. The bacterial culture was centrifuged at 5000 rpm for 10 min for cell separation from broth media. The remaining Cr (VI) concentration in the liquid media was determined using 1, 5-Diphenylcarbazide. The elimination of Cr (VI) from the liquid medium was analyzed using Equation (1).
%   Cr   ( VI )   removal = C o − C e C o × 100
where Co and Ce are the initial and final Cr (VI) concentrations in mg/L.

2.5. Statistical Analysis

All experiments in this research were performed in triplicate (n = 3) and graphs were constructed using the average experimental data value. The experimental errors (±standard deviation) were identified and plotted as error bars in graphs.

3. Result

3.1. Elemental Composition of Garden Soil

The availability of elements such as P, O, N, Ca, Si, and C was analyzed using XPS, as shown in Figure 1. The XPS analysis of garden soil showed the presence of oxygen at 539.08–525.08 eV, silica at 108.08–93.08 eV, phosphorus at 139–125 eV, carbon at 296–281 eV, calcium at 350.5–346.5 eV, and nitrogen at 409.08–391.08 eV. XPS analysis revealed that major peaks were observed for carbon and oxygen (Figure 1).

3.2. Cr (VI) Removal by Using Soil-Derived Microbial Consortia

The effects of Cr (VI) on bacterial growth and Cr (VI) removal efficiency are shown in Figure 2.
The bacterial cells were well grown in the control compared to Cr (VI)-containing media (Figure 2a). The bacterial cell showed delayed growth in the 100 mg/L Cr (VI)-containing media. The growth inhibition of bacterial cells in the heavy-metal-containing media confirmed the Cr (VI)’s toxicity to the bacterial cells.
The removal of Cr (VI) from the aqueous medium by bacterial mixed culture was observed, as shown in Figure 2b. The maximum removal of Cr (VI) was achieved as 99.37% at 100 mg/L Cr (VI) after 6 days of incubation. The minimum Cr (VI) removal (52.23%) on the first day and Cr (VI) removal was enhanced with incubation time, and maximum removal was reported on the sixth day.

3.3. High-Throughput Data Analysis

In the present study, the Illumina MiSeq sequencing platform was used for paired-end sequencing of DNA fragments. FastQC software revealed that metagenomic reads containing 56.5% GC content are shown in (Figure 3).
After prefiltering the datasets, metagenomic analysis of the garden soil sample shows the abundance of bacterial and archaeal microbial communities.

3.4. Taxonomic Composition Analysis

The metagenome sequence data were submitted to NCBI SRA under accession number SRR15186789 and BioProject number PRJNA747916. The taxonomy classification results consist of prokaryotes such as bacteria and archaea in the garden soil sample (Figure 4).
Figure 4 represents garden soil samples, mainly including Proteobacteria, Planctomycetes, Actinobacteria, Acidobacteria, Chloroflexi, Bacteroidetes, Firmicutes, Gemmatimonadetes, Nitrospirae, Verrucomicrobia, TM7, WS3, Chlamydiae, Elusimicrobia, Cyanobacteria, Chlorobi, OP3, Armatimonadetes, TM6, Spirochaetes, Tenericutes, Fusobacteria, Synergistetes, OP9, Thermotogae, Caldithrix, Thermi, and Euryarchaeota. Parvarchaeota and Crenarchaeota are also detected.
Proteobacteria was most abundant in the garden soil sample, followed by Planctomycetes, Actinobacteria, Acidobacteria, Chloroflexi, Bacteroidetes, and Firmicutes; the abundance of these bacteria indicated that these species play an essential role in the soil sample.
In this study, Gemmata, Planctomyces, Steroidobacter, Pirellula, Pedomicrobium, Rhodoplanes, Nitrospira, Mycobacterium, Pseudonocardia, Acinetobacter, Bdellovibrio, Kaistobacter, Candidatus Solibacter, Virgisporangium, Candidatus Entotheonella, Plesiocystis, Afifella, Anaerolinea, Virgisporangium, Agromyces, Actinoplanes, Hyphomicrobiium, Devosia, Bradyrhizobium, Agrobacterium, and Pseudomonas were present in garden soil (Figure 5).
In this study of soil samples, the most dominant genera—Gemmata, Planctomyces, Steroidobacter, Pirellula, Pedomicrobium, Rhodoplanes, Nitrospira, Mycobacterium, Pseudonocardia, and Acinetobacter—are shown in Figure 6.
Some of these genera were reported in the investigation of Walters et al. [45] on maize rhizobium. The highly enriched microbial community at the genus level shows their environmental characteristics, as depicted in Table 1.
The maximum abundant genus in garden soil shows their taxonomy and OTU number in Table 2.

4. Discussion

The XPS elemental analysis of soil confirmed the presence of O, C, Si, P, Ca, and N. Lopez-Nunez et al. [54] investigated elemental analysis in the soil and reported the presence of silica, calcium, and phosphorus in the soil sample. Zocche et al. [55] analyzed the heavy-metal composition in vegetable farming soil and reported silica, phosphorus, calcium, and zinc availability of the soil. Krupenikov et al. [56] reported elemental analysis in the clay soil and reported calcium and silica as major elements.
The growth of mixed bacterial culture was inhibited as the Cr (VI) concentration in the growth medium increased. Upadhyay et al. [57] isolated Bacillus sp. MNU16 from coal-mining water and reported that the bacterial isolate could be grown at high concentrations of Cr (VI). Masood and Malik [58] observed that Bacillus sp. FM1 growth was inhibited in the Cr (VI) containing medium compared to the control. Cr (VI) is attached to the bacterial surface in the growth medium and enters the cell via numerous cell-surface receptors [59]. Cr (VI) accumulates in the intracellular space of bacterial cells. The intracellular Cr (VI) is reduced into Cr (III), which is involved in the cell metabolic pathways and binds to the heavy binding protein [29].
These bacteria provide primary functions relevant to the biogeochemical cycle. Proteobacteria play critical roles in the nitrogen cycle, including nitrifying bacteria (Nitrospira) [60]. Iliev et al. [61] reported in their study that Proteobacteria were dominant in sediments or soils. Proteobacteria play an important role in the metabolic processes related to global carbon, nitrogen, and sulfur cycling in natural and artificial wetlands. The outcome of this study is similar to that of the study by Iliev et al. [61] on wetland soil. According to Gupta et al. [17], Proteobacteria were more prevalent in garden soil (61.74%) than in hospital soil (47.28%). Among Proteobacteria, Rhizobiales were enriched in the garden soil samples. This group was recognized to perform an essential role in nitrogen fixation. This can correlate with increased nitrogen content in garden soil. According to some researchers, garden soil has the highest microbial diversity of any soil [17]. Planctomycetes are the second most common bacteria in our samples. Actinobacteria are the third most common bacteria and play an important role in soil breakdown, humus construction, and nitrogen fixation in the soil system. Actinobacteria members are also economically and agriculturally relevant as a source of antibiotics and pesticides [62,63]. Chloroflexi is a photosynthetic bacteria present in garden soil samples.
Environment-related taxa such as chemoautotrophs characterized in our study are involved in ammonium oxidation such as Nitrospira and Bacillus. Iron and manganese oxidation such as Pedomicrobium and Geobacter were identified in our study. These bacterial genera are also involved in N2 fixation [64]. Szymańska et al. [65] reported that Pedomicrobium, more frequent in sugar beet, represents Rhizobiales, an order known for organisms that establish beneficial interactions with plants which encompasses plentiful bacteria with nitrogen-fixing competence.
In our study, Gemmata was dominant in garden soil. Garg et al. [66] reported that the genus Gemmata was absent in imidacloprid-applied soil. Garg et al. [66] also reported that the soil microbial community of garden soil had higher microbial diversity, as reported. The garden soil microbial diversity is associated with plant resistance to pathogens [66].
Agromyces and Bradyrhizobium bacterial genera were also found in our study, which confirms the superior fertility of the garden soil sample. Wang et al. [67] reported that Bacillus, Agromyces, Lysobacte, Pseudonocardia, and Bradyrhizobium were found in the majority in the healthy soil sample. Authors also investigated that these bacteria improve soil nutrients, encouraging plant growth, and monitoring soil-borne diseases. Rhodoplanes bacteria were one another dominant bacterial genera found in the garden soil sample in our study. These bacteria are phototrophic bacteria present in the rhizosphere soil [49]. Srinivas et al. [49] reported that Rhodoplanes were isolated from the rhizosphere soil of paddy. Oliveira et al. [64] reported that Nitrospira is found in vegetated soil, including unfertilized grassland soil. These microorganisms are found in the area surrounded by vegetative plants and trees. Li et al. [50] investigated that Nitrospira is an abundant bacterium that plays an essential role in the nitrification of fertilized soils. Nitrospira is found in diverse environments and plays an important role in the nitrogen cycle [68,69]. Hruska and Kaevska [70] reported that mycobacterium is non-tuberculous in mycobacteria detected in soil. The soil was easily contaminated by fertilization with manure or liquid dung, or water contaminated by animal faeces.
Genera Mycobacterium and Pseudonocardia were found in our study within the Actinobacteria group. Mycobacterium are generally free-living saprophytes and are the causative agents of a broad spectrum of human diseases. Pseudonocardia is a healthy plant-associated bacteria that promotes plant growth [48]. Mycobacterium was significantly enriched in the beech rhizosphere in the two most acidic and nutrient-poor soils [51]. Sit et al. [52] reported that Pseudonocardia isolated from the soil are considered rare actinomycetes. Holmes et al. [48] investigated Pseudonocardia species associated with Acromyrmex ants and found evidence to support the concept that Pseudonocardia might be a potential source of novel antimicrobials. Because they aggressively cut new leaves and eat them, Acromyrmex are sometimes known as “leafcutter ants”.
The Genus Acinetobacter found in our study plays an important role in the degradation of various long-chain dicarboxylic acids and aromatic and hydroxylated aromatic compounds. Iliev et al. [61] reported that the genus Acinetobacter could transform nitrogen through heterotrophic nitrification and aerobic denitrification. Some bacterial species within Firmicutes are present in fewer amounts in the garden soil sample. Soil bacteria are essential for the decomposition of organic matter from plant products [71]. Nitrogen-fixing microbes are present in the soil and some plants, such as peas and beans. Without microbes, the carbon and nitrogen cycles would not exist [72,73].

5. Conclusions

This study evaluated the distribution of bacterial diversity in garden soil and the role of the soil-derived bacterial consortia in mitigating toxic Cr (VI) ions from wastewater. The most abundant genera in garden soils are Gemmata, Planctomyces, Steroidobacter, Pirellula, Pedomicrobium, Rhodoplanes, Nitrospira Mycobacterium, Pseudonocardia, and Acinetobacter. The garden soil bacteria were also associated with improving soil fertility and promoting plant growth. The elemental analysis of garden soil indicated that carbon and oxygen were abundant in the soil. Additionally, nitrogen, silica, phosphorous, and calcium were also present in the soil. The soil-derived bacterial consortia removed 99.37% Cr (VI) from the water. This study revealed that the soil microbial community could help promote plant growth, biodegradation of organic matter, and the removal of toxic Cr (VI) ions from wastewater.

Author Contributions

N.S.: Writing—original draft preparation, including figures and tables; Conceptualization. V.S. and S.N.R.: Writing—Reviewing and Editing. E.V. and M.P.S.: Supervision, Writing—Reviewing and Editing. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the manuscript.

Acknowledgments

The authors are grateful to the University of Allahabad, Prayagraj, India, for providing internet access, a workspace, and instrumentation facilities for this research work.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Rawat, N.; Joshi, G.K. Bacterial community structure analysis of a hot spring soil by next generation sequencing of ribosomal RNA. Genomics 2019, 111, 1053–1058. [Google Scholar] [CrossRef] [PubMed]
  2. Whitman, W.; Coleman, D.; Wiebe, W. Prokaryotes: The unseen majority. Proc. Natl. Acad. Sci. USA 1998, 95, 6578–6583. [Google Scholar] [CrossRef] [Green Version]
  3. Girvan, M.S.; Bullimore, J.; Pretty, J.N. Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl. Environ. Microbiol. 2003, 69, 1800–1809. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Franz, E.; Schijven, J.; de Roda Husman, A.M.; Blaal, H. Meta-regression analysis of commensal and pathogenic Escherichia coli survival in soil and water. Environ. Sci. Technol. 2014, 48, 6763–6771. [Google Scholar] [CrossRef] [PubMed]
  5. van Veen, J.A.; van Overbeek, L.S.; van Elsas, J.D. Fate and activity of microorganisms introduced into soil Microbiol. Mol. Biol. Rev. 1997, 61, 121–135. [Google Scholar]
  6. Wu, X.; Yang, J.; Ruan, H.; Wang, S.; Yang, Y.; Naeem, I.; Wang, L.; Liu, L.; Wang, D. The diversity and co-occurrence network of soil bacterial and fungal communities andtheir implications for a new indicator of grassland degradation. Ecol. Indic. 2021, 129, 107989. [Google Scholar] [CrossRef]
  7. Stenuit, B.; Agathos, S.N. Deciphering microbial community robustness through synthetic ecology and molecular systems synecology. Curr. Opin Biotechnol. 2015, 33, 305–317. [Google Scholar] [CrossRef]
  8. da C Jesus, E.; Marsh, T.; Tiedje, J.M.; de S Moreira, F.M. Changes in land use alter the structure of bacterial communities in Western Amazon soils. ISME J. 2009, 3, 1004–1011. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  9. Wakelin, S.; Macdonald, L.; Rogers, S.; Gregg, A.L.; Bolger, T.P.; Baldock, J.A. Habitat selective factors influencing the structural composition and functional capacity of microbial communities in agricultural soils. Soil Biol. Biochem. 2008, 40, 803–813. [Google Scholar] [CrossRef]
  10. Amann, R.I.; Ludwig, W.; Schleifer, K.H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 1995, 59, 143–169. [Google Scholar] [CrossRef]
  11. Handelsman, J. Metagenomics: Application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 2004, 68, 669–685. [Google Scholar] [CrossRef] [PubMed]
  12. Mocali, S.; Benedetti, A. Exploring research frontiers in microbiology: The challenge of metagenomics in soil microbiology. Res. Microbiol. 2010, 161, 497–505. [Google Scholar] [CrossRef] [PubMed]
  13. Rajendhran, J.; Gunasekaran, P. Strategies for accessing soil metagenome for desired applications. Biotechnol. Adv. 2008, 26, 576–590. [Google Scholar] [CrossRef] [PubMed]
  14. Hardwick, S.A.; Chen, W.Y.; Wong, T.; Kanakamedala, B.S.; Deveson, I.W.; Ongley, S.E.; Santini, N.S.; Marcellin, E.; Smith, M.A.; Nielsen, L.K.; et al. Synthetic microbe communities provide internal reference standards for metagenome sequencing and analysis. Nat. Commun. 2018, 9, 3096. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Stevenson, B.S.; Eichorst, S.A.; Wertz, J.T.; Schmidt, T.M.; Breznak, J.A. New strategies for cultivation and detection of previously uncultured microbes. Appl. Environ. Microbiol. 2004, 70, 4748–4755. [Google Scholar] [CrossRef] [Green Version]
  16. Rivera, M.C.; Izard, J. Promises and Prospects of Microbiome Studies, 1st ed.; Izard, J., Rivera, M.C., Eds.; Elsevier: London, UK, 2015; pp. 144–159. [Google Scholar]
  17. Gupta, S.; Kumar, M.; Kumar, J.; Ahmad, V.; Pandey, R.; Chauhan, N.S. Systemic analysis of soil microbiome deciphers anthropogenic influence on soil ecology and ecosystem functioning. Int. J. Environ. Sci. Technol. 2017, 14, 2229–2238. [Google Scholar] [CrossRef]
  18. Hemmat-Jou, M.H.; Safari-Sinegani, A.A.; Mirzaie-Asl, A.; Tahmourespour, A. Analysis of microbial communities in heavy metals-contaminated soils using the metagenomic approach. Ecotoxicology 2018, 27, 1281–1291. [Google Scholar] [CrossRef]
  19. Almeida, O.G.G.; De Martinis, E.C.P. Bioinformatics tools to assess metagenomic data for applied microbiology. Appl. Microbiol. Biotechnol. 2019, 103, 69–82. [Google Scholar] [CrossRef]
  20. Chiang, A.D.; Dekker, J.P. From the Pipeline to the Bedside: Advances and Challenges in Clinical Metagenomics. J. Infect. Dis. 2020, 221, S331–S340. [Google Scholar] [CrossRef]
  21. Zethof, J.H.T.; Bettermann, A.; Vogel, C.; Babin, D.; Cammeraat, E.L.H.; Solé-Benet, A.; Lázaro, R.; Luna, L.; Nesme, J.; Woche, S.K.; et al. Prokaryotic Community Composition and Extracellular Polymeric Substances Affect Soil Microaggregation in Carbonate Containing Semiarid Grasslands. Front. Environ. Sci. 2020, 8, 51. [Google Scholar] [CrossRef]
  22. de Lima Brossi, M.J.; Jiménez, D.J.; Cortes-Tolalpa, L.; van Elsas, J.D. Soil-Derived Microbial Consortia Enriched with Different Plant Biomass Reveal Distinct Players Acting in Lignocellulose Degradation. Microb. Ecol. 2016, 71, 616–627. [Google Scholar] [CrossRef] [PubMed]
  23. Zhang, J.; Wei, L.; Yang, J.; Ahmed, W.; Wang, Y.; Fu, L.; Ji, G. Probiotic Consortia: Reshaping the Rhizospheric Microbiome and Its Role in Suppressing Root-Rot Disease of Panax notoginseng. Front. Microbiol. 2020, 11, 701. [Google Scholar] [CrossRef] [PubMed]
  24. Wei, L.; Yang, J.; Ahmed, W.; Xiong, X.; Liu, Q.; Huang, Q.; Ji, G. Unraveling the Association between Metabolic Changes in Inter-Genus and Intra-Genus Bacteria to Mitigate Clubroot Disease of Chinese Cabbage. Agronomy 2021, 11, 2424. [Google Scholar] [CrossRef]
  25. Zhang, J.; Ahmed, W.; Dai, Z.; Zhou, X.; He, Z.; Wei, L.; Ji, G. Microbial Consortia: An Engineering Tool to Suppress Clubroot of Chinese Cabbage by Changing the Rhizosphere Bacterial Community Composition. Biology 2022, 11, 918. [Google Scholar] [CrossRef]
  26. Phieler, R.; Voit, A.; Kothe, E. Microbially supported phytoremediation of heavy metal contaminated soils: Strategies and applications. Adv. Biochem. Eng. Biotechnol. 2014, 141, 211–235. [Google Scholar]
  27. Singh, V.; Singh, M.P.; Mishra, V. Bioremediation of toxic metal ions from coal washery effluent. Desalin. Water Treat. 2020, 197, 300–318. [Google Scholar] [CrossRef]
  28. Singh, V.; Singh, J.; Mishra, V. Development of a cost-effective, recyclable and viable metal ion doped adsorbent for simultaneous adsorption and reduction of toxic Cr (VI) ions. J. Environ. Chem. Eng. 2021, 9, 105124. [Google Scholar] [CrossRef]
  29. Singh, V.; Mishra, V. Microbial Removal of Cr (VI) by a New Bacterial Strain Isolated from the Site Contaminated with Coal Mine Effluents. J. Environ. Chem. Eng. 2021, 9, 106279. [Google Scholar] [CrossRef]
  30. Singh, V.; Singh, J.; Mishra, V. Sorption kinetics of an eco-friendly and sustainable Cr (VI) ion scavenger in a batch reactor. J. Environ. Chem. Eng. 2021, 9, 105125. [Google Scholar] [CrossRef]
  31. Singh, V.; Mishra, V. Sustainable reduction of Cr (VI) and its elemental mapping on chitosan coated citrus limetta peels biomass in synthetic wastewater. Sep. Sci. Technol. 2021, 57, 1609–1626. [Google Scholar] [CrossRef]
  32. Qasem, N.A.A.; Mohammed, R.H.; Lawal, D.U. Removal of heavy metal ions from wastewater: A comprehensive and critical review. npj Clean Water 2021, 4, 36. [Google Scholar] [CrossRef]
  33. Bazrafshan, E.; Mohammadi, L.; Ansari-Moghaddam, A.; Mahvi, A.H. Heavy metals removal from aqueous environments by electrocoagulation process—A systematic review. J. Environ. Health Sci. Eng. 2015, 13, 74. [Google Scholar] [CrossRef] [PubMed]
  34. Li, M.H.; Gao, X.Y.; Li, C.; Yang, C.L.; Fu, C.A.; Liu, J.; Wang, R.; Chen, L.X.; Lin, J.Q.; Liu, X.M.; et al. Isolation and Identification of Chromium Reducing Bacillus Cereus Species from Chromium-Contaminated Soil for the Biological Detoxification of Chromium. Int. J. Environ. Res. Public Health 2020, 17, 2118. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Lin, H.; You, S.; Liu, L. Characterization of Microbial Communities, Identification of Cr(VI) Reducing Bacteria in Constructed Wetland and Cr(VI) Removal Ability of Bacillus cereus. Sci. Rep. 2019, 9, 12873. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Singh, N.; Singh, M.P. Computational analysis of microbial community using amplicon sequencing of 16S rRNA gene. Res. J. Biotechnol. 2022, 17, 143–150. [Google Scholar] [CrossRef]
  37. Singh, N.; Singh, V.; Singh, M.P. Microbial degradation of lignocellulosic biomass for bioenergy production: A metagenomic-based approach. Biocatal. Biotransform. 2022. [Google Scholar] [CrossRef]
  38. Zhou, J.; Bruns, M.A.; Tiedje, J.M. DNA recovery from soils of diverse composition. Appl. Environ. Microbiol. 1996, 62, 316–322. [Google Scholar] [CrossRef] [Green Version]
  39. Singh, R.; Devi, T.; Verma, V.; Rasool, S. Comparative studies on the extraction of metagenomic DNA from various soil and sediment samples of Jammu and Kashmir region in prospect for novel biocatalysts. IOSR J. Environ. Sci. Toxicol. Food Technol. 2014, 8, 46–56. [Google Scholar]
  40. Ahmed, W.; Dai, Z.; Zhang, J.; Li, S.; Ahmed, A.; Munir, S.; Liu, Q.; Tan, Y.; Ji, G.; Zhao, Z. Plant-Microbe Interaction: Mining the Impact of Native Bacillus amyloliquefaciens WS-10 on Tobacco Bacterial Wilt Disease and Rhizosphere Microbial Communities. Microbiol. Spectr. 2022, 10, e0147122. [Google Scholar] [CrossRef]
  41. Andrews, S. FastQC: A Quality Control Tool for High Throughput Sequence Data. 2020. Available online: http://www.bioinformatics.babraham.ac.uk/projects/fastqc (accessed on 3 May 2020).
  42. Babraham Bioinformatics—TrimGalore! 2020. Available online: https://www.bioinformatics.babraham.ac.uk/projects/trim_galore/ (accessed on 3 May 2020).
  43. DeSantis, T.Z.; Hugenholtz, P.; Larsen, N. Greengenes, a Chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 2006, 72, 5069–5072. [Google Scholar] [CrossRef] [Green Version]
  44. Caporaso, J.G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F.D.; Costello, E.K.; Fierer, N.; Peña, A.G.; Goodrich, J.K.; Gordon, J.I. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7, 335–336. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  45. Walters, W.A.; Jin, Z.; Youngblut, N.; Wallace, J.G.; Sutter, J.; Zhang, W.; González-Peña, A.; Peiffer, J.; Koren, O.; Shi, Q. Large-scale replicated field study of maize rhizosphere identifies heritable microbes. Proc. Natl. Acad. Sci. USA 2018, 115, 7368–7373. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Wang, J.; Jenkins, C.; Webb, R.I. Isolation of Gemmata-like and Isosphaera-like planctomycete bacteria from soil and freshwater. Appl. Environ. Microbiol. 2002, 68, 417–422. [Google Scholar] [CrossRef] [PubMed]
  47. Gong, Z.L.; Zhang, C.F.; Jin, R.; Zhang, Y.Q. Steroidobacter flavus sp. nov., a microcystin-degrading Gammaproteobacterium isolated from soil. Antonie Van Leeuwenhoek 2016, 109, 1073–1079. [Google Scholar] [CrossRef]
  48. Holmes, N.A.; Innocent, T.M.; Heine, D.; Bassam, M.A.; Worsley, S.F.; Trottmann, F.; Patrick, E.H.; Yu, D.W.; Murrell, J.C.; Schiøtt, M. Genome Analysis of Two Pseudonocardia Phylotypes Associated with Acromyrmex Leafcutter Ants Reveals Their Biosynthetic Potential. Front. Microbiol. 2016, 7, 2073. [Google Scholar] [CrossRef] [Green Version]
  49. Srinivas, A.; Sasikala, C.; Ramana, C.V. Rhodoplanes oryzaesp. nov., a phototrophicalphaproteobacterium isolated from the rhizospheresoil of paddy. Int. J. Syst. Evol. Microbiol. 2014, 64, 2198–2203. [Google Scholar] [CrossRef]
  50. Li, C.; Hu, H.W.; Chen, Q.L.; Chen, D.; He, J.Z. Comammox Nitrospira play an active role in nitrification of agricultural soils amended with nitrogen fertilizers. Soil Biol. Biochem. 2019, 138, 107609. [Google Scholar] [CrossRef]
  51. Busti, E.; Monciardini, P.; Cavaletti, L.; Bamonte, R.; Lazzarini, A.; Sosio, M.; Donadio, S. Antibiotic-producing ability by representatives of a newly discovered lineage of actinomycetes. Microbiology 2006, 152, 675–683. [Google Scholar] [CrossRef] [Green Version]
  52. Sit, C.S.; Ruzzini, A.C.; Van Arnam, E.B.; Ramadhar, T.R.; Currie, C.R.; Clardy, J. Variable genetic architectures produce virtually identical molecules in bacterial symbionts of fungus-growing ants. Proc. Natl. Acad. Sci. USA 2015, 112, 13150–13154. [Google Scholar] [CrossRef] [Green Version]
  53. Jung, J.; Park, W. Acinetobacter species as model microorganisms in environmental microbiology: Current state and perspectives. Appl. Microbiol. Biotechnol. 2015, 99, 2533–2548. [Google Scholar] [CrossRef]
  54. Lopez-Nunez, R.; Ajmal-Poley, F.; González-Pérez, J.A.; Bello-López, M.A.; Burgos-Doménech, P. Quick Analysis of Organic Amendments via Portable X-ray Fluorescence Spectrometry. Int. J. Environ. Res. Public Health 2019, 16, 4317. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  55. Zocche, J.J.; Rohr, P.; Damiani, A.P.; Leffa, D.D.; Martins, M.C.; Zocche, C.M.; Teixeira, K.O.; Borges, G.D.; Jesus, M.M.; Santos, C.E.I.D.; et al. Elemental composition of vegetables cultivated over coal-mining waste. An. Acad. Bras. Cienc. 2017, 89, 2383–2398. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. Krupenikov, I.A.; Boincean, B.P.; Dent, D. Soil Mineralogy and Elemental Composition. In The Black Earth. International Year of Planet Earth; Springer: Dordrecht, The Netherlands, 2011. [Google Scholar] [CrossRef]
  57. Upadhyay, N.; Vishwakarma, K.; Singh, J. Tolerance and Reduction of Chromium (VI) by Bacillus sp. MNU16 Isolated from Contaminated Coal Mining Soil. Front. Plant Sci. 2017, 8, 778–790. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  58. Masood, F.; Malik, A. Hexavalent chromium reduction by Bacillus sp. strain FM1 isolated from heavy-metal contaminated soil. Bull. Environ. Contam. Toxicol. 2011, 86, 114–119. [Google Scholar] [CrossRef] [PubMed]
  59. Yilmazer, P.; Saracoglu, N. Bioaccumulation and biosorption of copper(II) and chromium(III) from aqueous solutions by Pichia stipitis yeast. J. Chem. Technol. Biotechnol. 2009, 84, 604–610. [Google Scholar] [CrossRef]
  60. Feng, G.; Xie, T.; Wang, X.; Bai, J.; Tang, L.; Zhao, H.; Wei, W.; Wang, M.; Zhao, Y. Metagenomic analysis of microbial community and function involved in cd-contaminated soil. BMC Microbiol. 2018, 18, 11. [Google Scholar] [CrossRef] [Green Version]
  61. Iliev, I.; Marhova, M.; Kostadinova, S.; Gochev, V.; Tsankova, M.; Ivanova, A.; Yahubyan, G.; Baev, V. Metagenomic analysis of the microbial community structure in protected wetlands in the Maritza River Basin. Biotechnol. Biotechnol. Equip. 2019, 33, 1721–1732. [Google Scholar] [CrossRef] [Green Version]
  62. Barka, E.A.; Vatsa, P.; Sanchez, L.; Gaveau-Vaillant, N.; Jacquard, C.; Meier-Kolthoff, J.P.; Klenk, H.P.; Clément, C.; Ouhdouch, Y.; van Wezel, G.P. Taxonomy, Physiology, and Natural Products of Actinobacteria. Microbiol. Mol. Biol. Rev. 2015, 80, 1–43. [Google Scholar] [CrossRef] [Green Version]
  63. Bond, J.G.; Marina, C.F.; Williams, T. The naturally derived insecticide spinosad is highly toxic to Aedes and Anopheles mosquito larvae. Med. Vet. Entomol. 2004, 18, 50–56. [Google Scholar] [CrossRef]
  64. Oliveira, C.; Gunderman, L.; Coles, C.A.; Lochmann, J.; Parks, M.; Ballard, E.; Glazko, G.; Rahmatallah, Y.; Tackett, A.J.; Thomas, D.J. 16S rRNA Gene-Based Metagenomic Analysis of Ozark Cave Bacteria. Diversity 2017, 9, 31. [Google Scholar] [CrossRef] [Green Version]
  65. Szymańska, S.; Sikora, M.; Hrynkiewicz, K.; Tyburski, J.; Tretyn, A.; Golebiewski, M. Choosing source of microorganisms and processing technology for next generation beet bioinoculant. Sci. Rep. 2021, 11, 2829. [Google Scholar] [CrossRef] [PubMed]
  66. Garg, N.; Bhattacherjee, A.K.; Shukla, P.K.; Singh, B. Influence of imidacloprid on bacterial community diversity of mango orchard soil assessed through 16S rRNA sequencing-based metagenomic analysis. Environ. Monit. Assess. 2021, 193, 102. [Google Scholar] [CrossRef] [PubMed]
  67. Wang, R.; Zhang, H.; Sun, L.; Qi, G.; Chen, S.; Zhao, X. Microbial community composition is related to soil biological and chemical properties and bacterial wilt outbreak. Sci. Rep. 2017, 7, 343. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  68. Lucker, S.; Wagner, M.; Maixner, F.; Pelletier, E.; Koch, H.; Vacherie, B.; Rattei, T.; Damsté, J.S.; Spieck, E.; Le Paslier, D. A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc. Natl. Acad. Sci. USA 2010, 107, 13479–13484. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  69. Van Kessel, M.A.H.J.; Speth, D.R.; Albertsen, M.; Nielsen, P.H.; Op den Camp, H.J.; Kartal, B.; Jetten, M.S.; Lücker, S. Complete nitrification by a single microorganism. Nature 2015, 528, 555–559. [Google Scholar] [CrossRef] [Green Version]
  70. Hruska, K.; Kaevska, M. Mycobacteria in water, soil, plants and air: A review. Vet. Med. 2012, 57, 623–679. [Google Scholar] [CrossRef] [Green Version]
  71. Jimenez-Perez, M.; Morales-Manzo, I.I.; Fita, A.; Rodriguez-Burruezo, A. Mitigation of drought stress in solanaceae vegetables through symbiosis with plant growth—Promoting bacteria and arbuscular mycorrhizal fungi. A review. AgroLife Sci. J. 2022, 11, 86–98. [Google Scholar]
  72. Fierer, N.; Leff, J.W.; Adams, B.J.; Caporaso, J.G. Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc. Natl. Acad. Sci. USA 2012, 109, 21390–21395. [Google Scholar] [CrossRef]
  73. Suciu, L.; Tarau, A.; Urda, C.; Chetan, F.; Muresanu, F.; Sopterean, L.; Boiu-Sicuia, O.A.; Barbu, L.D.N. The influence of bacterial inoculats on pathogens, yield and quality in soybean crop. AgroLife Sci. J. 2021, 10, 221–226. [Google Scholar]
Life 12 02094 g001 550
Figure 1. XPS survey of garden soil sample.
Figure 1. XPS survey of garden soil sample.
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Figure 2. Effect of Cr (VI) on bacterial growth (a) and Cr (VI) removal using bacterial microbial consortia (b).
Figure 2. Effect of Cr (VI) on bacterial growth (a) and Cr (VI) removal using bacterial microbial consortia (b).
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Figure 3. Using FastQC tools, we show the GC Content of the garden soil sample. Yellow line indicates to the theoretical distribution and green line indicates to the GC counts per read.
Figure 3. Using FastQC tools, we show the GC Content of the garden soil sample. Yellow line indicates to the theoretical distribution and green line indicates to the GC counts per read.
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Figure 4. Relative abundance of all bacterial and archaeal phylum in the garden soil sample.
Figure 4. Relative abundance of all bacterial and archaeal phylum in the garden soil sample.
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Figure 5. Show the microorganism at the genus level in garden soil.
Figure 5. Show the microorganism at the genus level in garden soil.
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Figure 6. Top 10 abundant genera in garden soil samples.
Figure 6. Top 10 abundant genera in garden soil samples.
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Table
Table 1. Major microbial communities play an essential role in garden soil.
Table 1. Major microbial communities play an essential role in garden soil.
Bacteria (Genus)Function (Characteristics)References
GemmataChemoheterotrophic aerobes [46]
PlanctomycesIt is found in microbial fuel cell systems; it plays a role in bioconversion and energy-transfer processes.[46]
SteroidobacterAgar-degrading bacteria, [47]
PirellulaChemoheterotrophic aerobes play a role in the degradation of sulfated glycopolymers.[46]
PedomicrobiumMore dominant in the crop field rhizosphere. Primarily found in sugar beet. It shows beneficial interaction with plants and comprises numerous bacteria with N2-fixing capability.[48]
RhodoplanesPhototrophic bacteria are present in the rhizosphere soil of paddy.[49]
NitrospiraThey are ubiquitous bacteria that play a role in the nitrification of fertilized soil.[50]
MycobacteriumIt is significantly enriched in the rhizosphere soil.[51]
PseudonocardiaIt is a plant-associated microbial community. It improves soil nutrients, promotes plant growth, and controls soil-borne disease. It also plays a vital role in the degradation of xylan through the production of xylanase.[52]
AcinetobacterIt implies active participation in the nutrient cycle in the ecosystem. It involves the degradation of various long-chain dicarboxylic acids and aromatic and hydroxylated aromatic compounds associated with plant degradation products.[53]
Table
Table 2. Most abundant microbial diversity of garden soil sample.
Table 2. Most abundant microbial diversity of garden soil sample.
OTU NumberKingdomPhylumClassOrderFamilyGenus
910BacteriaPlanctomycetesPlanctomycetiaGemmatalesGemmataceaeGemmata
679BacteriaPlanctomycetesPlanctomycetiaPlanctomycetalesPlanctomycetaceaePlanctomyces
424BacteriaProteobacteriaGammaproteobacteriaXanthomonadalesSinobacteraceaeSteroidobacter
BacteriaPlanctomycetesPlanctomycetiaPirellulalesPirellulaceaePirellula
257BacteriaProteobacteriaAlphaproteobacteriaRhizobialesHyphomicrobiaceaePedomicrobium
208BacteriaProteobacteriaAlphaproteobacteriaRhizobialesHyphomicrobiaceaeRhodoplanes
156BacteriaNitrospiraeNitrospiraNitrospiralesNitrospiraceaeNitrospira
119BacteriaActinobacteriaActinobacteriaActinomycetalesMycobacteriaceaeMycobacterium
119BacteriaActinobacteriaActinobacteriaActinomycetalesPseudonocardiaceaePseudonocardia
115BacteriaProteobacteriaGammaproteobacteriaPseudomonadalesMoraxellaceaeAcinetobacter
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Singh, N.; Singh, V.; Rai, S.N.; Vamanu, E.; Singh, M.P. Metagenomic Analysis of Garden Soil-Derived Microbial Consortia and Unveiling Their Metabolic Potential in Mitigating Toxic Hexavalent Chromium. Life 2022, 12, 2094. https://doi.org/10.3390/life12122094

AMA Style

Singh N, Singh V, Rai SN, Vamanu E, Singh MP. Metagenomic Analysis of Garden Soil-Derived Microbial Consortia and Unveiling Their Metabolic Potential in Mitigating Toxic Hexavalent Chromium. Life. 2022; 12(12):2094. https://doi.org/10.3390/life12122094

Chicago/Turabian Style

Singh, Nidhi, Veer Singh, Sachchida Nand Rai, Emanuel Vamanu, and Mohan P. Singh. 2022. "Metagenomic Analysis of Garden Soil-Derived Microbial Consortia and Unveiling Their Metabolic Potential in Mitigating Toxic Hexavalent Chromium" Life 12, no. 12: 2094. https://doi.org/10.3390/life12122094

APA Style

Singh, N., Singh, V., Rai, S. N., Vamanu, E., & Singh, M. P. (2022). Metagenomic Analysis of Garden Soil-Derived Microbial Consortia and Unveiling Their Metabolic Potential in Mitigating Toxic Hexavalent Chromium. Life, 12(12), 2094. https://doi.org/10.3390/life12122094

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